Watermelon mosaic virus (WMV, genus Potyvirus) is a significant pathogen affecting cucurbit production in the Western Black Sea and Central Anatolia regions of Türkiye, with limited knowledge of its genetic diversity hindering molecular control strategies. In this study, 19 complete coat protein (CP) gene sequences from WMV isolates collected from four cucurbit species were analyzed using RT-PCR, MEGA11 for phylogenetics, and DnaSP v6.12.03 for population genetics. The phylogenetic analysis, including 48 global isolates, classified eight Turkish isolates into the “emerging” (EM) group, 11 into the “classic” (G1) group, and identified a novel minor phylogroup. While a recombination signal was detected in isolate KP164988, none was observed in the Turkish isolates. Genetic diversity analysis showed that the G1 group was less divergent than the EM group, with all populations under strong purifying selection (ω = 0.022–0.243) and displaying recent expansion, likely due to variations in newly reported isolates. The results emphasize the genetic separation between EM and G1 groups and reveal frequent gene flow between Turkish and global populations. This comprehensive survey provides valuable insights into the genetic structure and diversity of WMV in Türkiye, supporting other reports on minor phylogroups within the virus populations.